Abstract
Basidiomycetes fungi have been utilized for the production of several compounds with bioactive properties, such as phenolic compounds. The present work quantified and identified the phenolic compounds produced in a kinetic study (63 days) and evaluated the antimicrobial activity from the extract obtained by Ganoderma lipsiense cultivation in solid-state fermentation using red rice. Phenolic compounds were identified by high-performance liquid chromatography–electrospray ionization tandem mass spectrometry (HPLC–ESI–MS/MS) and caffeic acid content was measured by high-performance liquid chromatography with diode-array detection (HPLC–DAD). Caffeic and syringic acids were produced by G. lipsiense. In the control medium (red rice), the following compounds were identified: p-coumaric acid, salicylic acid, ferulic acid and vanillin. High concentrations of caffeic acid (0.977 µg g−1) were measured in 49 days. Antimicrobial activity was investigated against Escherichia coli, Pseudomonas aeruginosa and Staphylococcus aureus using a minimum inhibitory concentration (MIC) technique. Ganoderma lipsiense extract was only effective against P. aeruginosa. These data have proved to be satisfactory in the study of biosynthesis of caffeic acid and antibacterial compounds by G. lipsiense in solid-state fermentation with red rice.
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Zárate-Chaves CA, Romero-Rodríguez MC, Niño-Arias FC, Robles-Camargo J, Linares-Linares M, Rodríguez-Bocanegra MX, Gutiérrez-Rojas I (2013) Optimizing a culture medium for biomass and phenolic compounds production using Ganoderma lucidum. Braz J Microbiol 44:215–223. https://doi.org/10.1590/S1517-83822013005000032
Ferreira ICFR, Heleno SA, Reis FS, Stojkovic D, Queiroz MJRP, Vasconcelos MH, Sokovic M (2015) Chemical features of Ganoderma polysaccharides with antioxidant, antitumor and antimicrobial activities. Phytochemistry 114:38–55. https://doi.org/10.1016/j.phytochem.2014.10.011
Tel-Çayan G, Öztürk M, Duru ME, Rehman MU, Adhikari A, Türkoğlu A, Choudhary MI (2015) Phytochemical investigation, antioxidant and anticholinesterase activities of Ganoderma adspersum. Ind Crops Prod 76:749–754. https://doi.org/10.1016/j.indcrop.2015.07.042
Tan X, Sun J, Xu Z, Li H, Hu J, Ning H, Qin Z, Pei H, Sun T, Zhang X (2018) Effect of heat stress on production and in vitro antioxidant activity of polysaccharides in Ganoderma lucidum. Bioprocess Biosyst Eng 41:135–141. https://doi.org/10.1007/s00449-017-1850-7
Rokem JS (2009) In: Doelle HW, Rokem S, Berovic M (eds) Biotechnology fundamentals in biotechnology, vol. 4EOLSS Publishers/UNESCO, Oxford
Steudler S, Bley T (2015) Biomass estimation during macro-scale solid-state fermentation of basidiomycetes using established and novel approaches. Bioprocess Biosyst Eng 38:1313–1323. https://doi.org/10.1007/s00449-015-1372-0
Mena P, Llorach R (2017) New frontiers on the metabolism, bioavailability and health effects of phenolic compounds. Molecules 22:151. https://doi.org/10.3390/molecules22010151
Wu ZM, Yu ZJ, Cui ZQ, Peng LY, Li HR, Zhang CL, Shen HQ, Yi PF, Fu BD (2017) In vitro antiviral efficacy of caffeic acid against canine distemper virus. Microb Pathog 110:240–244. https://doi.org/10.1016/j.micpath.2017.07.006
Lin Y, Yan Y (2012) Biosynthesis of caffeic acid in Escherichia coli using its endogenous hydroxylase complex. Microb Cell Fact 11:42. https://doi.org/10.1186/1475-2859-11-42
Dewick PM (2002) Medicinal natural products. A biosynthetic approach, 2nd edn. Wiley, West Sussex
Singdevsachan SK, Patra JK, Tayung K, Thatoi H (2017) Chemical constituents, antioxidative and antibacterial properties of medicinal mushrooms collected from Similipal Biosphere Reserve, Odisha, India. Proc Natl Acad Sci India Sect B Biol Sci 87:559–570. https://doi.org/10.1007/s40011-015-0574-1
Costa TM, Hermann KL, Garcia-Roman M, Valle RCSC, Tavares LBB (2017) Lipase production by Aspergillus niger grown in different agro-industrial wastes by solid-state fermentation. Braz J Chem Eng 34:419–427. https://doi.org/10.1590/0104-6632.20170342s20150477
Adolfo Lutz Institute (2008) Métodos físico-químicos para análise de alimentos, 5th edn. Instituto Adolfo Lutz, São Paulo
Thiex NJ, Manson H, Anderson S, Persson JA (2002) Determination of crude protein in animal feed, forage, grain and oilseeds by using block digestion with a copper catalyst and steam distillation into boric acid: collaborative study. J AOAC Int 85:309–317
Anagnostopoulou MA, Kefalas P, Papageorgiou VP, Assimopoulou AN, Boskou D (2006) Radical scavenging activity of various extracts and fractions of sweet orange peel (Citrus sinensis). Food Chem 94:19–25. https://doi.org/10.1016/j.foodchem.2004.09.047
CLSI (2012) Performance standards for antimicrobial susceptibility testing: twenty-second informational supplement. Clin Lab Stand Inst 32(3):M100-S22
Tenfen A, Siebert DA, Spudeit D, Mendes de Cordova CM, Micke GA, Alberton MD (2017) Determination of phenolic profile by HPLC-ESI-MS/MS and antibacterial activity of Eugenia platysema against mollicutes strains. J Appl Pharm Sci 7:7–11. https://doi.org/10.7324/JAPS.2017.70502
Wen D, Li C, Di H, Liao Y, Liu H (2005) A universal HPLC method for the determination of phenolic acids in compound herbal medicines. J Agric Food Chem 53:6624–6629. https://doi.org/10.1021/jf0511291
Costa Bde O, Nahas E (2012) Growth and enzymatic responses of phytopathogenic fungi to glucose in culture media and soil. Braz J Microbiol 43:332–340. https://doi.org/10.1590/S1517-838220120001000039
Zaghi LL Jr, Linde GA, Colauto NB (2010) Carbon-to-nitrogen ratios for Agaricus brasiliensis on the axenic method. Acta Sci Agron 32:55–60. https://doi.org/10.4025/actasciagron.v32i1.508610.4025/actasciagron.v32i1.5086
Walter M, Marchesan E (2011) Phenolic compounds and antioxidant activity of rice. Braz Arch Biol Technol 54:371–377. https://doi.org/10.1590/S1516-89132011000200020
Vieira GRT, Liebl M, Tavares LBB, Paulert R, Smânia A Jr (2008) Submerged culture conditions for the production of mycelial biomass and antimicrobial metabolites by Polyporus tricholoma Mont. Braz J Microbiol 39:561–568. https://doi.org/10.1590/S1517-838220080003000029
Denison SH (2000) pH regulation of gene expression in fungi. Fungal Genet Biol 29:61–71. https://doi.org/10.1006/fgbi.2000.1188
Peñalva MA, Arst HN Jr (2002) Regulation of gene expression by ambient pH in filamentous fungi and yeasts. Microbiol Mol Biol Rev 66:426–446
Haider K, Martin JP (1967) Synthesis and transformation of phenolic compounds by Epicoccum nigrum in relation to humic acid formation. Soil Sci Soc Am J 31:766–772. https://doi.org/10.2136/sssaj1967.03615995003100060019x
Bernats M, Juhna T (2015) Factors governing degradation of phenol in pharmaceutical wastewater by white-rot fungi: a batch study. Open Biotechnol J 9:93–99. https://doi.org/10.2174/1874070701509010093
Friedman M, Jürgens HS (2000) Effect of pH on the stability of plant phenolic compounds. J Agric Food Chem 48:2101–2110. https://doi.org/10.1021/jf990489j
Jayasinghe C, Imtiaj A, Hur H, Lee GW, Lee TS, Lee UY (2008) Favorable culture conditions for mycelial growth of Korean wild strains in Ganoderma lucidum. Mycobiology 36:28–33. https://doi.org/10.4489/MYCO.2008.36.1.028
Hasnat MA, Pervin M, Lim BO (2013) Acetylcholinesterase inhibition and in vitro and in vivo antioxidant activities of Ganoderma lucidum grown on germinated brown rice. Molecules 18:6663–6678. https://doi.org/10.3390/molecules18066663
Smania EFA, Monache FD, Yunes RA, Paulert R, Smania A Jr (2007) Antimicrobial activity of methyl australate from Ganoderma australe. Braz J Pharm 17:14–16. https://doi.org/10.1590/S0102-695X2007000100004
Mehta S, Jandaik S (2012) In vitro comparative evaluation of antibacterial activity of fruiting body and mycelial extracts of Ganoderma lucidum against pathogenic bacteria. J Pure Appl Microbiol 6:1997–2001
Yayan J, Ghebremedhin B, Rasche K (2015) Antibiotic resistance of Pseudomonas aeruginosa in pneumonia at a single University Hospital Center in Germany over a 10-year period. PLoS ONE 10:1–20. https://doi.org/10.1371/journal.pone.0139836
Choi JH, Kim S (2018) Mechanisms of attenuation of clot formation and acute thromboembolism by syringic acid in mice. J Funct Foods 43:112–122. https://doi.org/10.1016/j.jff.2018.02.004
Hasnat MA, Pervin M, Cha KM, Kim SK, Lim BO (2015) Anti-inflammatory activity on mice of extract of Ganoderma lucidum grown on rice via modulation of MAPK and NF-jB pathways. Phytochemistry 114:125–136. https://doi.org/10.1016/j.phytochem.2014.10.019
Cai S, Wang O, Wu W, Zhu S, Zhou F, Ji B, Gao F, Zhang D, Liu J, Cheng Q (2012) Comparative study of the effects of solid-state fermentation with three filamentous fungi on the total phenolics content (TPC), flavonoids, and antioxidant activities of subfractions from oats (Avena sativa L.). J Agric Food Chem 60:507–513. https://doi.org/10.1021/jf204163a
Karaman M, Jovin E, Malbaša R, Matavuly M, Popović M (2010) Medicinal and edible lignicolous fungi as natural sources of antioxidative and antibacterial agents. Phytother Res 24:1473–1481. https://doi.org/10.1002/ptr.2969
Olennikov DN, Tankhaeva LM, Agafonova SV (2011) Antioxidant components of Laetiporus sulphureus (Bull.: Fr.) Murr. fruit bodies. Appl Biochem Microbiol 47:419–425. https://doi.org/10.1134/S0003683811040107
Alvarado IE, Navarro D, Record E, Asther M, Asther M, Lesage-Meessen L (2003) Fungal biotransformation of p-coumaric acid into caffeic acid by Pycnoporus cinnabarinus: an alternative for producing a strong natural antioxidant. World J Microbiol Biotechnol 19:157–160. https://doi.org/10.1023/A:1023264200256
Edlin DAN, Narbad A, Dickinson JR, Lloyd D (1994) The biotransformation of simple phenolic compounds by Brettanomyces anomalus. FEMS Microbiol Lett 125:311–316
Acknowledgements
The authors are grateful to the Coordination for the Improvement of Higher Education Personnel (CAPES) Brazil, for financial support (Code 001). The authors D. Oliveira and L.B.B. Tavares are fellowship holders of the National Council for Scientific and Technological Development (CNPq).
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Costa, T.M., Kaufmann, V., Paganelli, C.J. et al. Kinetic identification of phenolic compounds and potential production of caffeic acid by Ganoderma lipsiense in solid-state fermentation. Bioprocess Biosyst Eng 42, 1325–1332 (2019). https://doi.org/10.1007/s00449-019-02131-8
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DOI: https://doi.org/10.1007/s00449-019-02131-8